The feasibility of developing a risk assessment for the impact of climate change on the emergence of Crimean-Congo haemorrhagic fever in livestock in Europe: a Review


Paul Gale, Veterinary Laboratories Agency, Weybridge, New Haw, Addlestone, Surrey, KT15 3NB, UK. E-mail:


Crimean-Congo haemorrhagic fever virus (CCHFV) is one of the most widespread of all medically important arboviruses with ticks of the Hyalomma spp. serving as the main vectors. Infection of livestock by CCHFV serves as a route of exposure to humans, as a reservoir of disease and as a route of importation. This study discusses the pathways and data requirements for a qualitative risk assessment for the emergence of CCHFV in livestock in Europe. A risk map approach is proposed based on layers that include the potential routes of release (e.g. by migrating birds carrying infected ticks) together with the main components for exposure, namely the distributions of the tick vectors, the small vertebrate host reservoirs and the livestock. A layer on landscape fragmentation serves as a surrogate for proximity of livestock to the tick cycle. Although the impact of climate change on the emergence of CCHF is not clear, comparing the distribution of risk factors in each layer currently with those predicted in the 2080s with climate change can be used to speculate how potential high-risk areas may shift. According to the risk pathway, transstadial and/or transovarial transmission in the tick vector are crucial for CCHFV spread. Vector competence and tick vector switching, however, remain critical factors for CCHFV colonization of new regions in Europe. The species of migratory bird is also an important consideration in the release assessment with greater abundance and biodiversity of ground-dwelling birds in southern Europe than in northern Europe.


Crimean-Congo haemorrhagic fever (CCHF) is one of the most widely distributed tick-borne diseases in the world, affecting people in the parts of Africa, Asia, eastern Europe and the Middle East (Ergonul and Whitehouse 2007). The causative agent, CCHF virus (CCHFV), is the second most widespread of all medically important arboviruses after dengue. It belongs to the genus Nairovirus in the family Bunyaviridae (Ergonul and Whitehouse 2007) and circulates in nature in a tick–vertebrate–tick cycle. CCHFV is transmitted by ticks of the genus Hyalomma, in particular Hyalomma marginatum. Antibodies against CCHFV have been detected in numerous small wild mammals including European hare (Lepus europaeus) and house mouse (Mus musculus) (Nalca and Whitehouse 2007). Humans are normally infected either through the bite of an infected tick, or through contact with a host infected with CCHFV during the acute phase of infection. The probability of getting the disease and becoming clinically ill for human subjects who have been infected with CCHFV is around 20% (Ergonul 2007) with case fatality rates reported as 5% in Turkey and 33% in Kosovo (Ergonul and Whitehouse 2007). Several recent outbreaks of CCHF have occurred in Turkey (see Randolph and Ergonul 2008) and clusters of cases have been observed recently in Balkan countries. Therefore, from a European Union (EU) perspective, it is important to understand the geographical areas that are suitable for transmission and how this risk will be altered in the future as a result of changes to climate, land use and socio-economic conditions. The objective of this study is to assess the feasibility of mapping regions in the EU where endemic CCHFV transmission may occur and how they are projected to change in the future with climate change.

The importance of livestock in CCHFV epidemiology

CCHF is listed as a notifiable disease by the World Organization for Animal Health, Office International des Epizooties (OIE 2006) because of its zoonotic importance. However, CCHFV infection does not cause severe clinical signs in livestock, and infection is generally subclinical. Antibodies against CCHFV have been detected in the sera of domestic animals such as cow (Bos taurus), donkey (Equus asinus), horse (Equus caballus), goat (Capra aegagrus hircus), sheep (Ovis aries) and pig (Sus scrofa) in regions of Europe, Asia and Africa (Hassanein et al. 2004; Nalca and Whitehouse 2007).

CCHFV infection in livestock is nevertheless important for a number of reasons. First, the high prevalence of antibodies against CCHFV and negligible levels of clinical disease among domestic animals in endemic regions suggest these animals are an important part of the ecology of CCHFV, if only to provide a blood meal to support transstadially infected adult ticks. Domestic ruminants may also develop a transmissible viraemia following infection (Nalca and Whitehouse 2007), and hence amplify the pathogen in agricultural environments, thus serving as a reservoir for infection of feeding adult ticks. Second, the importation of CCHFV-infected livestock (together with adult H. marginatum ticks) from endemic areas is one route by which the virus could be introduced into the EU. Third, the virus may be spread to butchers and abattoir workers through contact with blood or tissues from viraemic livestock during their slaughter and butchering. The distribution of human CCHF cases may vary seasonally. Thus, in Xinjiang (China) the majority of human cases occur between March and July each year perhaps reflecting the seasonal increases in CCHFV load in naïve newborn sheep (Saijo 2007). Studies of CCHF risk factors in Turkey suggest that high sero-positive rates in livestock are protective for humans (Ozkul 2009). The sero-positive rates of 400 cattle tested in Turkey were up to 79% (Ozkul 2009). This is consistent with infection of naïve livestock being an important factor in transmission of the virus to humans.

The impact of global and environmental changes on vector-borne diseases

Predicted climate change scenarios across Europe in the 2080s may be described broadly as higher temperatures particularly in southern Europe, increasing frequency of hot summers, a wetter northern Europe, a drier southern Europe and more extreme weather conditions with increased risks of heat wave, drought and flooding (IPCC 2001a,b; Beniston and Diaz 2004; Christensen and Christensen 2003).

The origins of emerging infectious diseases are correlated with socio-economic, environmental and ecological factors. Climate change may impact on livestock diseases through its effects on a number of factors including the range and abundance of vectors and wildlife reservoirs, survival of the pathogen in the environment and farming practice (Gale et al. 2009a). These factors may interact with each other and also with social and anthropogenic changes, including habitat destruction and changes in land use, which occur both globally and locally. The importance of climate change in the emergence of tick-borne diseases is not clear. Other factors such as social, political and economic changes are likely to have driven the emergence of tick-borne encephalitis virus (TBEV), for example, in the Baltic States since the 1990s (Sumilo et al. 2006). Climatic conditions are important for tick-to-tick transmission of TBEV (Rogers and Randolph 2006), and the effects of climate on human behaviour, and consequently on the rate at which humans are exposed to infected ticks, are believed to have resulted in the increase in tick-borne encephalitis (TBE) occurrence observed in some areas of Europe in 2006 (Randolph et al. 2008). Recent retrospective investigations did not confirm a potential role of climate change for the emergence of CCHF in Turkey in 2001 or in the Crimea in 1944 (Randolph 2008; Randolph and Ergonul 2008). Instead, an increase in the hare populations because of abandonment of hunting and growth of weeds in fields after reduction in agriculture because of terrorist activity in 2001 and war in 1944 were discussed as reasons for increased densities of Hyalomma ticks and the vertebrate host reservoirs.

Risk assessment approach

The risk assessment approach proposed in this article is based on the World Organization for Animal Health framework (see Gale et al. 2009b) which includes a release, exposure and consequence assessment. The release assessment describes the risk of entry of the virus into each EU member state (MS) from other regions of the world or from those EU MS in which CCHF is currently enzootic/endemic. The exposure assessment defines the risk of exposure of uninfected ticks, wildlife and livestock to CCHFV via different routes following virus release in an EU MS. The consequence assessment determines the risk of infection given exposure through each route. Human exposure was not considered for this assessment. The risk question is ‘What is the risk of incursion of CCHFV and establishment of endemicity in livestock in the EU at the current time and in the future given climate change?’ The risk pathway is set out in Fig. 1. The exposure and consequence assessments in effect represent a cycle between ticks, wildlife and livestock given release of the virus into the EU MS.

Figure 1.

 Risk pathway for Crimean-Congo haemorrhagic fever virus (CCHFV) in the European Union (EU). Note the risk to humans is not included at this stage. Main data requirements: (1) prevalence of CCHFV outside EU, (2) frequency of entry of CCHFV in ticks, (3) frequency of entry of CCHFV in wildlife, (4) frequency of entry of CCHFV in livestock, (5) survival and moult of tick, (6) probability of ticks’ feeding on migrant wildlife, (7) probability of ticks’ feeding on imported livestock, (8) abundance of CCHFV-infected ticks, (9) rate of transstadial and/or transovarial transmission, (10) probability of ticks’ feeding on native livestock, (11) probability of ticks’ feeding on indigenous wildlife, (12) tick-to-tick transmission, (13) abundance of susceptible ticks, (14) initiation of infection and virogenesis of the virus in the vector, (15) risk of susceptible livestock being infected through bite from infected tick and (16) risk of susceptible wildlife being infected through bite from infected tick.

The release assessment

Gale et al. (2009b) elicited expert opinion to assess the impact of climate change on the risks of incursion of CCHFV into the EU. The predicted risks through three routes studied, namely entry of CCHFV through infected tick vectors, wildlife and livestock were estimated qualitatively to be non-negligible. These three routes are therefore considered here in the release assessment (Fig. 1). The predicted risks through infected persons, pets and meat and meat products were estimated to be negligible and are not considered here (Gale et al. 2009b). A qualitative or quantitative assessment of the likelihood of ticks, wildlife or livestock entering EU MS being infected with CCHFV may be made depending on the degree of information available (i.e. presence/absence or prevalence of CCHFV) from the country of origin (1 in Fig. 1).

Hyalomma marginatum is a two-host tick (Hillyard 1996; Ergonul and Whitehouse 2007). The larvae and nymphs feed on small mammals (such as hares, hedgehogs and rodents) and ground-feeding birds (Hillyard 1996; Randolph and Rogers 2007) while adults feed on larger mammals such as livestock and wild boar (S. scrofa) in Europe (Ruiz-Fons et al. 2006). In Spain, the immature H. marginatum stages have been found on a number of bird species; the adults on cow, donkey, fox (Vulpes vulpes), boar and hare (Hillyard 1996). In one national park in South Africa, there was complete separation between immature stages of two Hyalomma tick species on hares (the most highly infested host species), ground-feeding birds or small rodents, and adult ticks on zebra and eland (cited by Randolph and Rogers 2007). The long duration of host attachment during the preimaginal development (12–26 days) enables the passive transport of the immature Hyalomma stages by migrating birds (Hillyard 1996) over long distances. Movement of cattle with adult H. marginatum ticks from the Balkans into central Europe is a potential route of release of CCHFV-infected adult ticks. Hyalomma marginatum is a common ectoparasite of horses in southern Europe, and the potential role of horses in importing adults into Great Britain (GB) has been highlighted recently (Jameson and Medlock 2009). To assess the probability of infected ticks entering a MS (pathway 2 in Fig. 1) requires data on the frequency of occurrence of Hyalomma ticks on migratory wild animals (birds and mammals) and imported livestock (including horses) and the origin of those ticks and their hosts. Pathways 3 and 4 (Fig. 1) represent entry of viraemic wildlife and livestock into the EU MS. Given that testing for CCHFV in livestock imported into the EU is not undertaken, data are required on the numbers of livestock imported together with their origins and transport routes.

The exposure assessment

Pathway 5 in Fig. 1 represents moult and survival of the infected immature tick once introduced into the EU MS, or survival in the case of introduced adult ticks. Pathways 6 and 7 in Fig. 1, meanwhile, represent the exposure of indigenous uninfected susceptible ticks to infected migrant wildlife and imported livestock, respectively, which enter the EU. The probabilities of indigenous ticks’ successfully questing and feeding on migrant birds or imported livestock are likely to vary in different parts of the EU and seasonally. Furthermore, questing by Ixodes ricinus, for example, may now occur throughout the winter in parts of Germany because of higher temperatures (Suss et al. 2008). Quantitative data on ticks collected from livestock and animals are now being gathered in GB under the tick recording scheme (Jameson and Medlock 2009). More specific information on how long the imported livestock remain in an EU MS, for example, before slaughter or transport elsewhere, and on the behaviour and habitats adopted by migrant wildlife would be required.

Central to the exposure assessment is the acarological risk determined by the pool of indigenous ticks infected with CCHFV (8 in Fig. 1). This will vary greatly not only between different EU MS but also within individual EU MS, reflecting the abundance and distribution of suitable tick vectors. The ability to transmit CCHFV between hosts has been demonstrated experimentally for H. marginatum but not for I. ricinus (see Turell 2007). Hard ticks such as H. marginatum and I. ricinus feed only once during each developmental stage (larva, nymph, and adult) (Turell 2007). Therefore to serve as a vector, the tick must ingest virus at one stage, become infected, transmit the virus transstadially or transovarially to the next stage, and then transmit the virus horizontally by bite to another vertebrate host during feeding (Turell 2007). Data are required on the rates and efficiencies of transovarial and transstadial transmissions for CCHFV in different tick species. Transovarial transmission and transstadial transmission of CCHFV are represented by pathway 9 (see Fig. 1). Transovarial transmission has been demonstrated for H. marginatum in nature (see Turell 2007 for review).

Pathway 10 (see Fig. 1) represents ticks’ feeding on native livestock with pathway 11 representing ticks on indigenous wildlife. Data are required on the rates of contact of ticks with wildlife and livestock. The indigenous wildlife reservoirs on which the ticks may feed will include nonmigratory mammals (e.g. small rodents, hares and hedgehogs) and resident bird species together with the migrant wildlife population that coincide at that time of the year in the area considered under pathway 6 (see Fig. 1). The data requirements for 6 and 11 will therefore be different and may well reflect different seasons of the year. In contrast, assuming imported livestock are treated similarly to national livestock the data for 7 and 10 may be similar.

Pathway 14 represents initiation of infection and virogenesis of the virus in the tick vector. This requires data on the probability that virogenesis occurs in the tick to give sufficient titres to infect a vertebrate host. There is no evidence that tick competence is affected by temperature in the same way as bluetongue virus in Culicoides midges (see Rogers and Randolph 2006). The smaller cycle indicated by pathways 9, 11, 12, 14 (Fig. 1) and confined to the exposure assessment represents tick-to-tick nonviraemic transmission, in which the virus is transmitted from an infected tick to an uninfected tick cofeeding on the same vertebrate host, without that host becoming viraemic. It has been shown (Gordon et al. 1993) that larval Hyalomma ticks become infected with CCHFV when cofed with infected adults of the same species, and that the CCHFV infection in those larvae infected by cofeeding was then able to be transmitted transstadially to the next nymph stage (pathway 9 in Fig. 1). Turell (2007) writes that the rates of transstadial transmission from those stages infected by cofeeding were very low in the study of Gordon et al. (1993). However, it should be noted that 0·6% of adult Hyalomma truncatum ticks (12 of 2049) were infected transstadially after developing from larvae exposed through cofeeding (Gordon et al. 1993). Of those larvae exposed directly through cofeeding, 0·8% (3 of 370) was infected. Thus, the percentage of adults infected is only slightly less than the percentage of larvae infected (0·6 vs 0·8%, respectively), suggesting transstadial transmission in H. truncatum at least, may be relatively efficient (i.e. 75%). It should be noted that the summary of Gordon et al. (1993) suggests 12 of 2049 adults represents 0·1% rather than 0·6%. Taken at face value, this could be misinterpreted as transstadial transmission being only 12% efficient.

The consequence assessment

The data requirements for the consequence assessment are the probabilities that an infected tick successfully infects a susceptible livestock animal or wild animal during feeding to give a viraemic reservoir of infection (pathways 15 and 16, respectively, in Fig. 1).

A geographical information system (GIS) approach to spatially represent potential high-risk areas within Europe

To develop a model based on Fig. 1 would be complex and there would be many data gaps. A more simple risk map approach is therefore proposed here based on layers that include the potential routes of release together with the main components for exposure.

Layer 1 – Map for risk of release of CCHFV into the EU

For the purposes of this assessment, a single route of release was considered, namely the entry of CCHFV-infected immature ticks on migratory wild birds (pathway 2 in Fig. 1). The aim of layer 1 of the risk assessment approach proposed here is to assess the spatial variability in the risk of release of CCHFV through this route into different regions of the EU. Layer 1 would further aim to capture the change in risk of release of CCHFV into the EU resulting from changes to the distribution or prevalence of CCHFV in those parts of the world where migrating birds winter or rest during migration.

The risk of release through wild birds needs to be addressed at the species level with regard to whether a particular species is likely to have landed in dry, shrub-type habitats in conditions suitable for survival and questing activity of the Hyalomma tick. Water/marsh birds would appear less likely to have been in the H. marginatum environment in the nonbreeding sites. In Spain, the immature stages of H. marginatum have been found on partridge (Perdix perdix), fieldfare (Turdus pilaris), magpie (Pica pica), little owl (Athene noctua), stone curlew (Burhinus oedicnemus) and buzzard (Buteo buteo) (Hillyard 1996). The five species of bird on which the immature H. marginatum ticks were detected in GB (Martyn 1988) were the sedge warbler (Acrocephalus schoenobaenus), whitethroat (Sylvia communis), whinchat (Saxicola rubetra), northern wheatear (Oenanthe oenanthe) and redstart (Phoenicurus phoenicurus). Those species that could have migrated from CCHF-endemic areas should be listed, and maps obtained for their summer breeding ranges and abundances in Europe. For each species, an assessment of the likelihood of its origin being in CCHF-endemic areas should also be made. This requires information on the prevalence of CCHFV in the nonbreeding (wintering) grounds used by the species, together with the migration routes into Europe. The space-time overlapping of a certain species in a certain habitat could be inferred from the migration registers, which include dates for ringing/recovery registers and time between those registers. Ornithological databases such as those maintained by the Spanish Office of Migratory Species (OEM-MARM) are a key resource for assessing this component of risk, as such databases often contain information on the paths taken by migratory birds including stop-over locations. Satellite tracking has been used to map the migration of long-range migrants such as the white stork (Ciconia ciconia) through east Africa and the Balkans into central Europe (Berthold et al. 2004).

Predicting the impact of climate change on the range, diversity and abundance of European migrants

Information on how climate change, together with habitat loss and changing land use in the future, will affect both the wintering range and the breeding range of the migrant is important. Huntley et al. (2007, 2008) provide graphical representations in climate space of the European bird species’ distributions and map the predicted impact of climate change on range. The research of Gregory et al. (2009) indicates that climate change is already having a detectable Europe-wide effect at the level of a large avian species assemblage, with evidence that changes are positive for certain avian populations but negative for others. Specifically, for example, it has been shown that climate change is reducing the abundance of certain insectivorous, long-range migrants such as pied flycatchers (Ficedula hypoleuca) in northern Europe (Both et al. 2006). In GB and Ireland, there has been a marked retraction of the northern wheatear’s breeding range because of the habitat change (Shaw 2002). In the case of European Sylvia warblers, potential breeding ranges consistently showed a northwards shift with climate change with predicted migration distances increasing by double in the case of trans-Saharan migrant species (Doswald et al. 2009). Range-restricted species are expected to experience major population reductions because of the lack of overlap between their present and potential future ranges (Doswald et al. 2009). Overall, Doswald et al. (2009) predicted that migratory species will suffer greater negative impact from climate change than species that are resident or undertake only short-distance migrations. In addition, climate change might influence the migration behaviour strategy (Doswald et al. 2009) and migration routes of the birds thereby influencing also the transport of associated ticks.

Layer 2 – Probability of moult and survival of immature ticks on entering EU

Given that CCHFV-infected immature H. marginatum ticks have entered an EU MS, layer 2 maps the probability of their moult and survival. Because the immature hard ticks feed only once during each stage, an immature tick which arrives on a migrant bird would not feed again until its metamorphosis was complete, and thus would be a dead end for the virus if it failed to moult. The rate at which immature tick stages moult is determined by the accumulated temperature within their microclimate away from the host. The arrival of many migratory bird species in Europe during the spring (late March to mid April) may be too early for the climatic conditions to be suitable for completion of moult of the attached H. marginatum nymphs. However, the timing of migration varies by bird species and could be affected by climate change, allowing for larvae and nymph survival. Thus, for example, if the breeding range of a migrant shifts northwards because of climate change (Doswald et al. 2009), that migrant may arrive later in the season, although the effect may be mitigated by the lower temperatures at more northerly latitudes. The risk of exposure of susceptible animals to CCHFV-infected ticks imported on migrant birds could be increased in the parts of Europe by the following reasons:

  • 1 very warm weather occurring in late March/mid April. In addition, there might be specific regions with microclimates sufficient for tick moult (e.g. in the Rhine Rift in Germany). A more local view is needed to identify these regions;
  • 2 the migrant birds’ arriving later in the year, e.g. May, June, July. This does happen with a few late arrivals both at the species level and the individual level. For example, there are certain migrant bird species, such as common swift (Apus apus) that arrive in northern Europe later than mid April. It should be noted, however, that swifts do not land on the ground as they cannot take off again, and exposure to Hyalomma ticks would be unlikely.

Layer 3 – Distribution and density of tick vectors in Europe

Layer 3 should include data on the abundance (density), geographical distribution and habitat association of potential tick vectors of CCHFV in Europe. CCHFV has been isolated in nature from at least 30 tick species including H. marginatum, I. ricinus, Rhipicephalus sanguineus, Rhipicephalus turanicus, Rhipicephalus bursa and also from three Dermacentor tick spp. including Dermacentor marginatus (see Turell 2007). However, as discussed by Turell (2007), the mere isolation of virus from an arthropod does not incriminate it as an actual vector. Hyalomma marginatum is believed to be the main vector of CCHFV in the Balkans, Crimea and southern Russia (Estrada-Peña et al. 2007) and is abundant in southern Europe (Estrada-Peña and Venzal 2007). Ixodes ricinus is abundant in central and northern Europe (Randolph et al. 2008; Pietzsch et al. 2005). Rhipicephalus sanguineus and R. turanicus have been detected in the Netherlands recently (Nijhof et al. 2007). Rhipicephalus bursa is distributed across southern Europe (Estrada-Peña and Venzal 2007). Dermacentor marginatus is distributed in southern Europe, France, Switzerland, Germany and Poland (Hillyard 1996; Estrada-Peña and Venzal 2007). For some European countries (e.g. the Netherlands and Italy), ticks are well surveyed and mapped with accuracy (Cringoli et al. 2005; Nijhof et al. 2007). Some data are available for records in Europe not only for H. marginatum but also for D. marginatus, R. bursa and R. turanicus (Estrada-Peña and Venzal 2007).

There is a considerable research activity in understanding and predicting the distribution of tick species including R. bursa, R. turanicus and H. marginatum in the Mediterranean region (Estrada-Peña and Venzal 2007) and I. ricinus in Europe (Estrada-Peña 2008a). The main climatic variables influencing habitat suitability for ticks are the normalized difference vegetation index (NDVI) and land surface temperature (Sumilo et al. 2006; Estrada-Peña et al. 2007). Estrada-Peña et al. (2007) used data for climate and vegetation (temperature and NDVI) to develop a predictive model of the habitat suitability of H. marginatum in Turkey. The distribution of a tick vector species is probably not limited by the distribution of its hosts, e.g. deer and cattle (see Randolph 2000). Ticks occupy only a subset of their hosts’ ranges because a large part of a tick’s life cycle is spent on the ground (Estrada-Peña 2008a) where abiotic factors such as the vegetation and climate determine tick development and survival rates and hence set the broad-scale boundaries to their ranges. Humidity is a key factor affecting the survival of some tick species such as I. ricinus, which requires at least 80% humidity (see Pietzsch et al. 2005). Indeed, because of its relatively permeable cuticle, I. ricinus looses 50% of its body weight per day when exposed to dry air at 25°C (Hillyard 1996). In contrast, other tick species such as H. marginatum favour steppe and savanna environments with fairly low humidity (see Kampen et al. 2007). The availability of humid resting locations for adult ticks may vary over very short distances in certain land-cover types, as noted by Danielova et al. (2006) who described a particular (and common) habitat found in altitudes above 1000 m in the Krkonose Mountains (Czech Republic) consisting of a solitary tree or a small group of trees in grassy land with branches reaching the ground.

Predicting the impact of climate change on the range and distribution of Hyalomma marginatum

There is already evidence for the effect of climate change on the abundance, range and distribution of some tick species in Europe. Danielova et al. (2006) reported a marked vertical shift to higher altitudes (by up to 500 m) in the distribution of I. ricinus in mountains in the Czech Republic. Dautel et al. (2006) have concluded that Dermacentor reticulatus has expanded its range into northern Germany and the Netherlands, and climate change may be partly responsible (Gray et al. 2009). According to Suss et al. (2008), temperature conditions for ticks will continue to improve in large parts of Germany, especially in those regions in the south with the highest predicted increases in temperature, and climate suitability models predict that eight important tick species are likely to establish more northern permanent populations in a climate-warming scenario (Gray et al. 2009).

Ticks are constantly being introduced into new areas through movement and transport of wildlife, livestock, pets and other exotic animals, and perhaps even humans (Kampen et al. 2007). For such introduction events to result in establishment, the ticks need to survive, locate maintenance hosts and reproduce. Dogs transported from the south of France, Spain and Italy have introduced R. sanguineus into northern Europe (Hillyard 1996). Infestations of this hard tick have been reported within and outside GB quarantine kennels, with a case of its establishing in a well-heated house in London reported more than 20 years ago (see Gale et al. 2009a). Rhipicephalus species require temperatures above 18°C to complete their life cycle, and milder winters could facilitate their establishment in northern Europe. Some indication of the suitability of a region for the establishment of ticks can be obtained by studying the range of climates in which the species currently occurs elsewhere in its range. In one example study, daily climate data including mean, minimum and maximum temperatures, daily rainfall and potential evapotranspiration were obtained for some 6000 points in Europe and Africa where H. marginatum had been collected (Estrada-Peña 2008b). The author concluded that different populations were restricted by different climatic factors, and that a simple generalization about the effects of climate on different populations of H. marginatum ticks is not feasible. For instance, most southern populations (northern Africa) are restricted by high evaporation rates, while southern European populations are restricted by high rainfall and low evaporation. Only populations in the east of the range and those colonizing mountains are restricted by temperature in late autumn and early winter, probably affecting the moment of moult of immature stages. According to Estrada-Peña and Venzal (2007), the climate scenario that was most compatible with estimates of future climate in the Mediterranean region (increase in temperature and decrease in rainfall) was predicted to produce a northward expansion in the extent of suitable habitats for H. marginatum, R. bursa and R. turanicus. Areas of Europe with increased habitat suitability for H. marginatum after increased temperature and decreased rainfall include northern Spain and Portugal, France, Italy, the Balkans and coastal areas of Turkey.

Layer 4 – Distribution and density of small vertebrate host reservoirs

There are many small mammal reservoir species to consider. The main competent wildlife reservoirs for CCHFV in each EU MS need to be identified. It is proposed to consider the distributions and densities of the most abundant small vertebrate species dwelling in those habitats suitable for immature H. marginatum ticks. For adult ticks, larger mammals need to be considered together with livestock (see layer 5). The geographical distribution of each of these mammal species in Europe is documented by Mitchell-Jones et al. (1999), and databases are maintained by the Societas Europaea Mammalogica (2009). The abundance and densities of wild mammals in Europe fluctuate. In GB, there is some evidence that the brown rat (Rattus norvegicus) increased in abundance between 1996 and 2002, although large annual population fluctuations may obscure trends (Battersby 2005). Similarly, roe deer (Capreolus capreolus) and muntjac (Muntiacus reevesi) are increasing in abundance in GB (Battersby 2005). In Italy, both roe deer and red deer (Cervus elaphus) have increased their densities more than one order of magnitude in the last 50 years (Rizzoli et al. 2009). This may be related to changes in land and wildlife management practices. Rizzoli et al. (2009) argue that changes in the forest structure and composition (namely an increasing ratio of high stand forest to coppice cover) provide a suitable habitat for the yellow-necked mouse (Apodemus flavicollis) which is the species mainly responsible for nonviraemic (tick-to-tick) transmission of TBEV in alpine provinces of northern Italy. The structure and species composition of vegetation within a woodland influence the density and abundance of small mammals. In particular, the synchronous production of seeds occurring in high stand forests, but rarely in coppices, influences small rodent populations according to Rizzoli et al. (2009). Farming practice also affects wildlife abundance. For example, changes in farming practice in GB have resulted in a considerable decline in the abundance of the house mouse (Battersby 2005). Anthropogenic factors may result in an immigration of wildlife such as noncommensal rodents, wild boar and foxes into metropolitan areas of Europe.

Effect of climate change on small vertebrate reservoirs

Climate change may affect not only the range and abundance of wild vertebrates but also the biodiversity and behaviour of wildlife (see Gale et al. 2009a). In GB and northern Europe, increased precipitation may enhance food resources for small mammals with milder, damper microclimatic conditions and the absence of winter frosts, enabling them to feed on invertebrates throughout the winter. In the Mediterranean region of Italy, higher temperatures and lower precipitation have resulted in increases in thermoxerophilic mammal species, which could reduce biodiversity (Szpunar et al. 2008).

Layer 5 – Distribution of livestock

Good data sets are available for the distribution of livestock species across Europe. Current distributions of the major livestock species (cattle, buffalo, sheep, goats, pigs and poultry) are set out by FAO (2005) at a spatial resolution of three minutes of arc (c. 5 km). Changes in socio-economic and environmental (including climatic) factors may affect not only the distribution and the movement of livestock within the EU but also the specific breeds of livestock which are farmed.

Layer 6 – Proximity of livestock to the virus–vertebrate–tick cycle

Spatial proximity of livestock to the tick–vertebrate–tick cycle is an important requirement for the pathway in Fig. 1. This is supported by the work of Estrada-Peña et al. (2007) who identified not only climate suitability for the tick but also landscape fragmentation (through interspersion of agricultural land with shrub-type vegetation and forest) as important predictors of CCHF cases in humans in Turkey. Landscape fragmentation may be important through bringing humans and their livestock, vertebrate hosts and Hyalomma ticks into proximity such that humans and livestock intrude on the natural virus–tick–wild vertebrate cycle. Thus, Hyalomma ticks would favour the shrub-type vegetation, wild vertebrates would favour the forest edges and agricultural workers (together with livestock) would be in the adjacent fields. Habitat fragmentation patterns can be determined using vegetation data based on Landsat imagery (Estrada-Peña et al. 2007). Landscape fragmentation may be more important in eastern Europe than in western Europe.


Figure 1 presents the risk pathway for the infection of livestock with CCHFV in Europe. Obtaining specific data for each of the pathway steps is complex. Furthermore, because the immature Hyalomma tick stages feed on the smaller vertebrate wildlife while adults feed on larger wildlife species and livestock (see Randolph and Rogers 2007), the release and exposure pathways in Fig. 1 will require breaking down into separate routes for immature and adult tick stages with different data sets and parameters. A simplified GIS approach based on layers is therefore proposed. Comparing the distribution of risk factors in each layer currently with those predicted in the 2080s with climate change may indicate how potential high-risk areas will shift and so facilitate targeted surveillance. The resolutions of layers 3, 4 and 5 are not sufficient to accommodate the proximity required for exposure, and an additional layer 6 representing landscape fragmentation is proposed to represent areas of close contact of humans (and therefore their livestock) with ticks and wild vertebrate reservoirs. Layer 6 in effect represents social change. Information on changes in land use through terrorist or military activity could be included in other layers such as tick and wildlife abundance. Weighting of the layers through expert opinion will be an important part of the process.

The risk of a pathogen introduction resulting in an outbreak is often analysed via the concept of R0, the ‘basic reproductive ratio’, which quantifies the expected number of secondary infections arising from the introduction of a single infected individual into a naïve population. R0-based approaches to infectious disease risk assessments in general and tick-borne disease risk assessments in particular (Hartemink et al. 2008) are of great value as they integrate all elements of the transmission cycle and allow quantitative outputs to be generated. Indeed, the layers 2–6 identified earlier collectively describe most of the elements of R0 which are likely to vary spatially: the life histories of the vectors and the host populations, and the rate of contact between the two. In the event that accurate quantitative data are available in these areas, it would be possible to analyse the data in these layers to obtain an expression of the suitability of a region for CCHFV transmission in terms of R0. The approach taken here recognizes that quantitative information regarding all of these elements is very rarely available and is therefore designed to be capable of providing qualitative insights into transmission suitability even in the absence of a fully quantitative data set.

A H. marginatum rufipes tick was identified on a horse in the Netherlands during a survey of tick species (Nijhof et al. 2007). As that horse was not imported, it is speculated that the tick was introduced by a migratory bird. Hyalomma marginatum rufipes is endemic in many regions of Africa, and larvae or nymphs of this species have been encountered on migratory birds from Africa to Europe in spring (see Nijhof et al. 2007). Introduction of CCHFV into Turkey by migratory wild birds and livestock has been argued against by Randolph and Ergonul (2008). Indeed, bearing in mind that bird migration has been occurring for thousands of years, those authors rightly ask, ‘Why now?’. Predictions of the risks of introduction of H. marginatum ticks by birds are complicated by the high biodiversity and variation in abundances of migratory birds across Europe. Some ground-feeding bird species of dry, arid environments are long-range migrants whilst others are sedentary. Furthermore, the degree of migration may vary within a species depending on the breeding site location, the environmental conditions and the breeding status of the individuals (Terasse 2006). Of interest with regard to the introduction of H. marginatum ticks is the difference between southern and northern Europe in relation to breeding migrants coming from Africa. An initial inspection of the distribution of bird species would suggest greater abundance and biodiversity of ground-feeding, long-range migrant species breeding in southern Europe compared to northern Europe. This is consistent with the low level of detection of H. marginatum ticks on migratory birds in GB, for example. Thus Martyn (1988) reported only eight records of H. marginatum on newly arrived migrant warblers and chats in GB. Studies to quantify exotic tick species on migratory birds will provide useful information to validate predictions on those bird species likely to introduce H. marginatum ticks into EU countries. For example, Pietzsch et al. (2008) collected 38 ticks of four Ixodes species from 12 species of migratory bird in GB.

Until recently, all records of H. marginatum in north-west Europe (GB, France, Denmark and Norway) referred to larvae and nymphs, with adult ticks not having been detected. In early May 2006, however, a questing adult female H. marginatum tick was reported in southern Germany (Kampen et al. 2007). That tick was isolated on the clothing of a person who had been in rural surroundings in southern Germany and had also visited rural areas in central Spain some weeks prior. It is not clear whether that female tick had been imported as an adult, or as a larva/nymph which subsequently developed into an adult in Germany. In March 2009, importation of an adult (male) H. marginatum tick into GB was recorded on a horse imported from Portugal (Jameson and Medlock 2009). Migratory birds (even large species) are more likely to arrive with immature H. marginatum tick stages rather than adult ticks. The probability of survival and moult of immature H. marginatum ticks once released into different parts of Europe is thus an important consideration in the risk assessment. A case can be made for the current risk of CCHFV incursions (through release from infected ticks attached to migrating birds) into northern Europe being lower than for southern Europe. First, there is a greater abundance and biodiversity of those ground-dwelling birds which have migrated from sub-Saharan Africa in southern Europe compared to northern Europe; and second, temperatures in northern Europe may not be high enough for imported immature ticks attached to them to moult. Through climate change, however, some southern European bird species may expand their breeding ranges into more northern parts of Europe, and warming because of climate change may increase the chances of the moulting and survival of the immature ticks. Furthermore, higher temperatures and reduced rainfall in southern Europe may result in an increase in the proportion of dry shrub-type habitats suitable for H. marginatum, resulting in an expansion of its distribution northwards (Estrada-Peña and Venzal 2007). This expanded range may in turn mean that a higher proportion of those birds migrating to northern Europe are exposed to the tick during stopovers in southern Europe.

Tick-to-tick transmission is included in the exposure assessment (Fig. 1) and is important for the transmission of certain flaviviruses including TBEV (Rogers and Randolph 2006; Hartemink et al. 2008). It has been proposed that TBEV is susceptible to climate change because the fragile temporal synchrony between different tick stages required for cofeeding is broken (Rogers and Randolph 2006). The efficiency of tick-to-tick transmission for CCHFV in H. truncatum tick larvae cofed on guinea pig hosts is only 0·8% (Gordon et al. 1993) compared to 72% efficiency for TBEV in I. ricinus tick nymphs cofed on nonimmune A. flavicollis hosts (Labuda et al. 1997). Furthermore, the separation observed between immature tick stages of H. marginatum which prefer small mammals and birds, and the adult ticks which prefer larger mammals (cited by Randolph and Rogers 2007) would further diminish the opportunities for tick-to-tick transmission. Thus, transmission of CCHFV may not be susceptible to climate change in the same way as TBEV. This is consistent with the findings that recent emergence of CCHF in Turkey was not linked to climate change (Randolph 2008; Randolph and Ergonul 2008). The main drivers for the impact of climate change on the risk of CCHFV in Europe would appear to be through layers 1, 2 and 3, namely change in the range and abundance of migratory birds, change in the chances of immature ticks’ moulting and change in the range of the H. marginatum tick, respectively.

While H. marginatum is currently confined to southern Europe, I. ricinus is abundant in central and northern Europe. Vector competence and tick vector switching remain critical factors for CCHFV colonization of new regions in Europe. Potentially significant gaps in the data are in the competence of I. ricinus as a vector for CCHFV (pathway 14 in Fig. 1) and whether transstadial and/or transovarial transmission could occur so enabling the next life cycle stage of the I. ricinus tick to pass infection on to livestock or wildlife (pathway 9 in Fig. 1). Single mutations in the genomes of certain alphaviruses, including Chikungunya virus (Tsetsarkin et al. 2007) and Venezuelan equine encephalitis virus (Brault et al. 2004), allow a change of the mosquito vector species. CCHFV is a segmented, negative-sense RNA virus and could evolve rapidly through mutation and reassortment. Indeed, it is conceivable that socio-economic, environmental, climatic and ecological changes could provide a unique combination of factors creating a new niche for the evolution and emergence of CCHFV in indigenous tick species in northern and central Europe. However, although populations of RNA viruses are often remarkably diverse, it does not necessarily follow that they can easily respond to environmental challenges. Indeed, their evolution may be constrained when mutation rates reach an error threshold (Holmes 2003). In the case of arboviruses, such as CCHFV, the requirement to replicate in hosts that are as phylogenetically distinct as mammals and invertebrates may further constrain their evolution.

Climate change and other factors may reduce biodiversity in small vertebrate hosts. High vertebrate biodiversity appears to be an important factor in reducing transmission of zoonotic pathogens among wildlife hosts. Thus, both infection prevalence of hantaviruses in wild rodent populations and reservoir population density increased when small mammal species diversity was reduced by removing nonreservoir species in replicated field plots in Panama (Suzan et al. 2009). Swaddle and Calos (2008) found a lower incidence of West Nile virus in humans in eastern US counties that have greater avian (viral host) diversity when controlled for confounding factors. The potential impact of decreasing small mammal and bird biodiversity on the transmission dynamics of CCHFV is not known. An additional layer to accommodate the biodiversity of small vertebrates may refine the prediction.


This work was funded under work package 7.4 by EPIZONE, a Network of Excellence for Epizootic Disease Diagnosis and Control and partial funding from the European Union FP7 grant.